Apidologie 35 (2004) 619–622
© INRA/DIB-AGIB/ EDP Sciences, 2004
DOI: 10.1051/apido:2004053
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Original article
Interspecific differences in response to novel landmarks
in bumblebees (Bombus sp.)
Dave GOULSON*, Ben DARVILL, Jon ELLIS, Mairi E. KNIGHT, Mick E. HANLEY
Division of Biodiversity and Ecology, School of Biological Sciences, Biomedical Sciences Building,
Bassett Crescent East, Southampton SO16 7PX, UK
(Received 30 October 2003; revised 12 March 2004; accepted 19 March 2004)
Abstract – We provide evidence for interspecific differences in the behaviour of bumblebees which
suggests that there may be important differences in the way that they navigate. Bumblebees commonly
investigate the novel landmark presented by a human standing in open countryside. When doing so they
perform a characteristic flight similar to that observed when a naïve bee first leaves the nest, suggesting that
they are memorising the location of an unfamiliar landmark. We compare the frequency with which
different bee species perform this behaviour. Striking patterns emerge. Only workers of certain bumblebee
species were recorded investigating novel human landmarks, notably Bombus lapidarius and B. soroeensis.
Other species such as B. pascuorum, B. hortorum and B. pratorum never performed this behaviour, yet were
abundant in the study area. We suggest that this behaviour may be indicative of species with long foraging
ranges and therefore greater need to pay attention to landmarks.
Bombus / navigation / foraging range / memory
1. INTRODUCTION
Despite much research, our understanding
of the navigational abilities of animals remains
far from complete. Honeybees (Apis mellifera
L.) have received considerable attention in this
respect; they can navigate up to 20 km from
their nest in search of food, and are able to
remember and communicate the locations of
food sources (von Frisch, 1967; Seeley, 1985).
They are known to rely heavily on visual landmarks (Southwick and Buchmann, 1995; Dyer,
1996), and also use a sun compass to relate the
positions of landmarks and the nest (Wehner,
1994). They seem able to plot a direct trajectory
home following a complex outward route,
although exactly how they do this remains
* Corresponding author: [email protected]
unclear. Some authors claim that bees develop
“cognitive maps” of their landscape, although
this remains controversial (Gould, 1986; Dyer,
1991; Menzel, 2001).
Some bumblebee (Bombus sp.) species can
forage over several kilometres from their nests
(Goulson and Stout, 2001; Osbourne et al.,
2001; Walther-Hellwig and Frankl, 2000;
Goulson, 2003), but the upper limits of their
foraging range are not known. Marking experiments suggest that some species such as B.
muscorum mostly remain within 200 m of their
nests whilst others such as B. lapidarius and B.
terrestris forage further afield (Walther-Hellwig
and Frankl, 2000). Here we provide different
evidence that there may be important differences in navigation behaviour between species.
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When standing in the countryside in summer
it is common to be investigated by flying bumblebees, a phenomenon colloquially known as
“buzzing” (for brevity this term is adopted
here). The flying bee approaches to within 2–
4 m of the person and then flies from side to
side at a height of 2–4 m, describing a horizontal arc of increasing length. After perhaps 4 s
the bee performs a series of two to five loops
around the observer before flying away. This
behaviour can be observed frequently, particularly when standing in open countryside with
few obvious landmarks nearby.
Here we test whether bumblebees species
differ in the frequency with which they perform
this behaviour, by simultaneously comparing
the numbers of different bumblebee species
buzzing with the numbers observed in counts
on flowers.
Figure 1. Numbers of each bumblebee species
recorded on flowers versus buzzing, based on 46
one hour searches for bumblebees at sites scattered
across Salisbury Plain, southern UK. All castes
combined.
3. RESULTS AND DISCUSSION
2. METHODS
Our study was carried out in July and August
2002 and 2003 on Salisbury Plain Military Training
Area, UK. Salisbury Plain predominantly consists of
large areas of undulating unimproved grassland,
with few shrubs or trees and thus few natural landmarks. Forty six sites on the plain, each separated by
at least 1 km, were searched for one man hour. All
sites lay between 51° 06’ and 51° 20’ N and 1° 40’
and 2° 00’ W, and were between 150 and 200 m altitude. All bumblebees that were foraging on flowers
were recorded. Bees that buzzed the researchers
were netted and identified. It must be noted that
catching these bees is difficult, and the success rate
was probably less than 30%. Any bee that flew from
side to side, well above the vegetation, and while
next to the observer, was deemed to be buzzing. Bees
sometimes perform a similar behaviour when they
are disturbed when foraging by an observer; where
this was the case the bees were not classified as buzzing. The observers did not wear brightly-coloured
clothing so the bees were unlikely to have mistaken
the observer for an inflorescence, and bumblebees
almost never spontaneously attack humans. Thus the
buzzing behaviour was interpreted as being investigative. B. terrestris and B. lucorum where combined
since these two species are exceedingly hard to distinguish reliably in the field. A χ2 test was used to
examine whether the proportions of each bumblebee
species recorded buzzing differed from the overall
proportions of each species that were recorded at the
study site. Rare species in which the expected
number of bees recorded buzzing was less than five
were pooled.
One hundred and twenty three bumblebees
were caught and identified while buzzing,
while 1658 bumblebees were recorded foraging on flowers. In total 13 bumblebee species
were recorded, but only four of these were ever
recorded buzzing (B. lapidarius, B. soroeensis
and small numbers of B. terrestris/lucorum and
B. sylvarum) (Fig. 1). The proportions of each
species recorded buzzing differed significantly
between species (χ26 = 269, P < 0.001). All but
six of the 123 bees caught buzzing were workers, the remainder being 3 male B. lapidarius
and 3 male B. soroeensis. No cuckoo bumblebees (subgenus Psithyrus) were recorded buzzing. Species that were common but were never
recorded buzzing include B. pascuorum, B. humilis, B. hortorum, B. pratorum, B. rupestris and
B. vestalis. The incidence of buzzing does not
follow taxonomic groupings. The four species
which we recorded buzzing are all from separate subgenera of Bombus (Williams, 1998).
The present study suggests that there are
important differences in the behaviour of bumblebees that we do not as yet understand. It
seems probable that buzzing is related to navigation, and that buzzing bees are investigating
new landmarks. The behaviour seems to be
identical to that observed in naïve bees when
they first emerge from the nest (D.G. unpublished data), which fly from side to side in an
expanding arc while facing the nest entrance,
Interspecific differences in bumblebee navigation?
presumably to memorise its position. Thus we
hypothesize that buzzing bees are memorising
the location of a novel landmark. We envisage
that the behaviour occurs when a bee travelling
through familiar territory encounters a new
landmark, and pauses to add the position and
shape of this landmark to its memory.
Why should some species “buzz” but not
others? Even within those species recorded
buzzing, some appear to do it much more frequently than others. Nearly half of the B. soroeensis recorded were buzzing (46%), compared to
just 10% for B. lapidarius. What is the significance of these inter-specific differences?
Bumblebee species may differ in the range over
which they forage. Walther-Hellwig and Frankl
(2000) suggest that B. muscorum forage within
200 m of their nests whilst B. lapidarius and
B. terrestris regularly forage over > 1 km.
Using molecular markers to identify sisters, we
have recently found that B. terrestris workers
tend to range over greater distances than those
of B. pascuorum (Darvill et al., 2004). However, we do not have accurate estimates of
mean or variance in foraging range for any
bumblebee species. Presumably species that
forage further afield pay more attention to landmarks. The species that we recorded buzzing
broadly corresponds with those thought to have
a large foraging range (particularly B. lapidarius and B. terrestris), while B. pascuorum
(which has a shorter foraging range) was never
recorded buzzing. Little or nothing is known of
the foraging range of the other species in our
study, such as B. soroeensis. We know very little about the foraging range of most bumblebee
species despite it being a fundamental aspect of
their ecology. If there are big differences
between species, this could affect their susceptibility to habitat change or degradation, and
knowledge of foraging range would enable
habitat management for rarer species on an
appropriate scale. Clearly further research is
needed in this area, particularly on the less well
studied bumblebee species such as B. soroeensis.
Résumé – Différences interspécifiques en réponse
à de nouveaux repères topographiques chez les
bourdons (Bombus sp.). Il existe des preuves selon
lesquelles les bourdons (Bombus sp.) peuvent présenter
de grandes différences dans leur rayon de butinage,
bien qu’il s’agisse d’un comportement notoirement
difficile à quantifier. Nous apportons ici la preuve
qu’il existe des différences interspécifiques nettes
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dans le comportement des ouvrières de bourdons.
Cela suggère qu’il peut y avoir des différences
importantes dans la façon dont elles naviguent. Les
bourdons examinent communément un nouveau repère
topographique représenté par une personne debout
au milieu d’un espace ouvert. Ce faisant, ils exécutent un vol caractéristique semblable à celui que l’on
observe quand une abeille naïve quitte le nid pour la
première fois, suggérant qu’ils mémorisent l’emplacement d’un repère non familier. Nous avons comparé la fréquence avec laquelle différentes espèces
de bourdons présentaient ce comportement avec
l’abondance globale de chaque espèce mesurée
d’après des comptages sur les fleurs. L’étude a été
menée dans la plaine de Salisbury, dans le sud de
l’Angleterre, où existe une grande diversité d’espèces de bourdons. Les ouvrières de certaines espèces
seulement ont été vues examiner les nouveaux repères humains, notamment Bombus lapidarius et B.
soroensis, et occasionnellement B. terrestris/lucorum
et B. sylvarum (Fig. 1). Les autres espèces comme
B. pascuorum, B. hortorum et B. pratorum n’ont
jamais présenté ce comportement, pourtant ils étaient
présents en abondance sur le lieu d’étude. Nous suggérons que ce comportement peut être indicatif
d’espèces ayant un long rayon de butinage et donc
besoin d’une plus grande attention portée aux repères
topographiques.
Bombus / navigation / rayon de butinage /
mémoire
Zusammenfassung – Interspezifische Unterschiede
bei der Reaktion auf neue Landmarken bei Hummeln (Bombus sp.). Es gibt viele Hinweise darauf,
dass sich Hummelarten (Bombus Latr.) sehr stark in
der Größe ihres Sammelareals unterscheiden,
obwohl die Schwierigkeit einer Quantifizierung des
Sammelverhaltens altbekannt ist. Hier zeigen wir
Befunde, die auf einen deutlichen Unterschied im
Verhalten der Hummelarbeiterinnen zwischen den
Arten hinweisen. Sie deuten auf wichtige Unterschiede
in der Methode ihrer Navigation hin. Allgemein
erkunden Hummeln von Menschen aufgestellten
neuen Landmarken in der offenen Landschaft. Dabei
verfolgen sie eine typische Flugbahn ähnlich dem
ersten Orientierungsflug von jungen Bienen, was zur
Annahme führt, dass sie sich die unbekannten Landmarken einprägen. Wir verglichen die Frequenz dieses Verhaltens bei verschiedenen Hummelarten mit
ihrer durch Zählungen an Blüten erfassten Vorkommenshäufigkeit. Die Untersuchung wurden in der
Salisbury Ebene in Südengland durchgeführt, eine
Gegend mit einer hohen Diversität an Hummelarten.
Es ergaben sich erstaunliche Muster. Nur bestimmte
Hummelarten wurden bei der Inspizierung der neuen
für den Versuch errichteten Landmarken beobachtet, besonders häufig Bombus lapidarius und B.
soroeensis, und manchmal B. terrestris/lucorum und
B. sylvarum (Abb. 1). Andere Arten wie B. pascuorum, B. hortorum und B. pratorum zeigten niemals
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dieses Verhalten, obwohl sie in der Versuchsgegend
häufig vorkamen. Wir vermuten, dass dieses Verhalten
typisch für Arten mit einem großen Sammelgebiet
ist, die aus diesem Grund genauer auf die Landmarken achten müssen.
Bombus / Navigation / Sammelareal / Lernen
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